Skip to main content

Advertisement

SpringerLink
Log in

Differential role of Rac in the basolateral amygdala and cornu ammonis 1 in the reconsolidation of auditory and contextual Pavlovian fear memory in rats

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale and objectives

A conditioned stimulus (CS) is associated with a fearful unconditioned stimulus (US) in the traditional fear conditioning model. After fear conditioning, the CS–US association memory undergoes the consolidation process to become stable. Consolidated memory enters an unstable state after retrieval and requires the reconsolidation process to stabilize again. Evidence indicates the important role of Rac (Ras-related C3 botulinum toxin substrate) in the acquisition and extinction of fear memory. In the present study, we hypothesized that Rac in the amygdala is crucial for the reconsolidation of auditory and contextual Pavlovian fear memory.

Methods

Auditory and contextual fear conditioning and microinjections of the Rac inhibitor NSC23766 were used to explore the role of Rac in the reconsolidation of auditory and contextual Pavlovian fear memory in rats.

Results

A microinjection of NSC23766 into the basolateral amygdala (BLA) but not central amygdala (CeA) or cornu ammonis 1 (CA1) immediately after memory retrieval disrupted the reconsolidation of auditory Pavlovian fear memory. A microinjection of NSC23766 into the CA1 but not BLA or CeA after memory retrieval disrupted the reconsolidation of contextual Pavlovian fear memory.

Conclusions

Our experiments demonstrate that Rac in the BLA is crucial for the reconsolidation of auditory Pavlovian fear memory, whereas Rac in the CA1 is critical for the reconsolidation of contextual Pavlovian fear memory.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Amaral DG (2003) The amygdala, social behavior, and danger detection. Ann N Y Acad Sci 1000:337–47

    Article  PubMed  Google Scholar 

  • Bahar A, Dorfman N, Dudai Y (2004) Amygdalar circuits required for either consolidation or extinction of taste aversion memory are not required for reconsolidation. Eur J Neurosci 19:1115–8

    Article  PubMed  Google Scholar 

  • Baldi E, Mariottini C, Bucherelli C (2008) Differential roles of the basolateral amygdala and nucleus basalis magnocellularis during post-reactivation contextual fear conditioning reconsolidation in rats. Neurobiol Learn Mem 90:604–9

    Article  PubMed  Google Scholar 

  • Barak S, Liu F, Ben Hamida S, Yowell QV, Neasta J, Kharazia V, Janak PH, Ron D (2013) Disruption of alcohol-related memories by mTORC1 inhibition prevents relapse. Nat Neurosci 16:1111–7

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barnes P, Kirtley A, Thomas KL (2012) Quantitatively and qualitatively different cellular processes are engaged in CA1 during the consolidation and reconsolidation of contextual fear memory. Hippocampus 22:149–71

    Article  PubMed  Google Scholar 

  • Borrelli S, Musilli M, Martino A, Diana G (2013) Long-lasting efficacy of the cognitive enhancer cytotoxic necrotizing factor 1. Neuropharmacology 64:74–80

    Article  CAS  PubMed  Google Scholar 

  • Bucherelli C, Baldi E, Mariottini C, Passani MB, Blandina P (2006) Aversive memory reactivation engages in the amygdala only some neurotransmitters involved in consolidation. Learning & memory (Cold Spring Harbor, NY) 13:426–30

    Article  CAS  Google Scholar 

  • Cammarota M, Bevilaqua LR, Rossato JI, Lima RH, Medina JH, Izquierdo I (2008) Parallel memory processing by the CA1 region of the dorsal hippocampus and the basolateral amygdala. Proc Natl Acad Sci U S A 105:10279–84

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Campolongo P, Roozendaal B, Trezza V, Hauer D, Schelling G, McGaugh JL, Cuomo V (2009) Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proc Natl Acad Sci U S A 106:4888–93

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen C, Kim JJ, Thompson RF, Tonegawa S (1996) Hippocampal lesions impair contextual fear conditioning in two strains of mice. Behav Neurosci 110:1177–80

    Article  CAS  PubMed  Google Scholar 

  • Cingolani LA, Goda Y (2008) Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9:344–56

    Article  CAS  PubMed  Google Scholar 

  • Davis M (1992) The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15:353–75

    Article  CAS  PubMed  Google Scholar 

  • de la Fuente V, Freudenthal R, Romano A (2011) Reconsolidation or extinction: transcription factor switch in the determination of memory course after retrieval. J Neurosci 31:5562–73

    Article  PubMed  Google Scholar 

  • Debiec J, LeDoux JE, Nader K (2002) Cellular and systems reconsolidation in the hippocampus. Neuron 36:527–38

    Article  CAS  PubMed  Google Scholar 

  • Diana G, Valentini G, Travaglione S, Falzano L, Pieri M, Zona C, Meschini S, Fabbri A, Fiorentini C (2007) Enhancement of learning and memory after activation of cerebral Rho GTPases. Proc Natl Acad Sci U S A 104:636–41

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ding ZB, Wu P, Luo YX, Shi HS, Shen HW, Wang SJ, Lu L (2013) Region-specific role of Rac in nucleus accumbens core and basolateral amygdala in consolidation and reconsolidation of cocaine-associated cue memory in rats. Psychopharmacology 228:427–37

    Article  CAS  PubMed  Google Scholar 

  • Dudai Y (2006) Reconsolidation: the advantage of being refocused. Curr Opin Neurobiol 16:174–8

    Article  CAS  PubMed  Google Scholar 

  • Duvarci S, Nader K, LeDoux JE (2005) Activation of extracellular signal-regulated kinase- mitogen-activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning. Eur J Neurosci 21:283–9

    Article  PubMed  Google Scholar 

  • Elzinga BM, Bremner JD (2002) Are the neural substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)? J Affect Disord 70:1–17

    Article  CAS  PubMed  Google Scholar 

  • Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629–35

    Article  CAS  PubMed  Google Scholar 

  • Fanselow MS (2000) Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 110:73–81

    Article  CAS  PubMed  Google Scholar 

  • Ghashghaei HT, Barbas H (2002) Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115:1261–79

    Article  CAS  PubMed  Google Scholar 

  • Hall J, Thomas KL, Everitt BJ (2001) Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J Neurosci: Off J Soc Neurosci 21:2186–93

    CAS  Google Scholar 

  • Hellemans KG, Everitt BJ, Lee JL (2006) Disrupting reconsolidation of conditioned withdrawal memories in the basolateral amygdala reduces suppression of heroin seeking in rats. J Neurosci: Off J Soc Neurosci 26:12694–9

    Article  CAS  Google Scholar 

  • Hoeffer CA, Cowansage KK, Arnold EC, Banko JL, Moerke NJ, Rodriguez R, Schmidt EK, Klosi E, Chorev M, Lloyd RE, Pierre P, Wagner G, LeDoux JE, Klann E (2011) Inhibition of the interactions between eukaryotic initiation factors 4E and 4G impairs long-term associative memory consolidation but not reconsolidation. Proc Natl Acad Sci U S A 108:3383–8

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang W, Zhu PJ, Zhang S, Zhou H, Stoica L, Galiano M, Krnjevic K, Roman G, Costa-Mattioli M (2013) mTORC2 controls actin polymerization required for consolidation of long-term memory. Nat Neurosci 16:441–8

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huff ML, Miller RL, Deisseroth K, Moorman DE, LaLumiere RT (2013) Posttraining optogenetic manipulations of basolateral amygdala activity modulate consolidation of inhibitory avoidance memory in rats. Proc Natl Acad Sci U S A 110:3597–602

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hughes V (2012) Stress: the roots of resilience. Nature 490:165–7

    Article  CAS  PubMed  Google Scholar 

  • Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–69

    Article  CAS  PubMed  Google Scholar 

  • Jin XC, Lu YF, Yang XF, Ma L, Li BM (2007) Glucocorticoid receptors in the basolateral nucleus of amygdala are required for postreactivation reconsolidation of auditory fear memory. Eur J Neurosci 25:3702–12

    Article  PubMed  Google Scholar 

  • Johansen JP, Cain CK, Ostroff LE, LeDoux JE (2011) Molecular mechanisms of fear learning and memory. Cell 147:509–24

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kennedy MB, Beale HC, Carlisle HJ, Washburn LR (2005) Integration of biochemical signalling in spines. Nat Rev Neurosci 6:423–34

    Article  CAS  PubMed  Google Scholar 

  • Krettek JE, Price JL (1978) A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid axonal connections. J Comp Neurol 178:255–80

    Article  CAS  PubMed  Google Scholar 

  • LaLumiere RT, Buen TV, McGaugh JL (2003) Post-training intra-basolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. J Neurosci: Off J Soc Neurosci 23:6754–8

    CAS  Google Scholar 

  • LeDoux J (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23:727–38

    Article  PubMed  Google Scholar 

  • LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–84

    Article  CAS  PubMed  Google Scholar 

  • Lee JL (2009) Reconsolidation: maintaining memory relevance. Trends Neurosci 32:413–20

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee JL, Everitt BJ, Thomas KL (2004) Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science (New York, NY) 304:839–43

    Article  CAS  Google Scholar 

  • Li FQ, Xue YX, Wang JS, Fang Q, Li YQ, Zhu WL, He YY, Liu JF, Xue LF, Shaham Y, Lu L (2010) Basolateral amygdala cdk5 activity mediates consolidation and reconsolidation of memories for cocaine cues. J Neurosci: Off J Soc Neurosci 30:10351–9

    Article  CAS  Google Scholar 

  • Li YQ, Li FQ, Wang XY, Wu P, Zhao M, Xu CM, Shaham Y, Lu L (2008) Central amygdala extracellular signal-regulated kinase signaling pathway is critical to incubation of opiate craving. J Neurosci 28:13248–57

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lu L, Hope BT, Dempsey J, Liu SY, Bossert JM, Shaham Y (2005) Central amygdala ERK signaling pathway is critical to incubation of cocaine craving. Nat Neurosci 8:212–9

    Article  CAS  PubMed  Google Scholar 

  • Lu L, Uejima JL, Gray SM, Bossert JM, Shaham Y (2007) Systemic and central amygdala injections of the mGluR(2/3) agonist LY379268 attenuate the expression of incubation of cocaine craving. Biol Psychiatry 61:591–8

    Article  CAS  PubMed  Google Scholar 

  • Lubin FD, Sweatt JD (2007) The IkappaB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron 55:942–57

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Luo YX, Xue YX, Shen HW, Lu L (2013) Role of amygdala in drug memory. Neurobiol Learn Mem 105:159–73

    Article  CAS  PubMed  Google Scholar 

  • Luskin MB, Price JL (1983) The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J Comp Neurol 216:264–91

    Article  CAS  PubMed  Google Scholar 

  • Maddox SA, Watts CS, Schafe GE (2013) p300/CBP histone acetyltransferase activity is required for newly acquired and reactivated fear memories in the lateral amygdala. Learning & memory (Cold Spring Harbor, NY) 20:109–19

    Article  CAS  Google Scholar 

  • Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931

    Article  CAS  PubMed  Google Scholar 

  • Maren S (2005a) Building and burying fear memories in the brain. Neuroscientist: Rev J bringing Neurobiol, Neurol Psychiatry 11:89–99

    Article  Google Scholar 

  • Maren S (2005b) Synaptic mechanisms of associative memory in the amygdala. Neuron 47:783–6

    Article  CAS  PubMed  Google Scholar 

  • Maren S, Phan KL, Liberzon I (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14:417–28

    Article  CAS  PubMed  Google Scholar 

  • Martinez LA, Klann E, Tejada-Simon MV (2007) Translocation and activation of Rac in the hippocampus during associative contextual fear learning. Neurobiol Learn Mem 88:104–13

    Article  CAS  PubMed  Google Scholar 

  • McGaugh JL (1966) Time-dependent processes in memory storage. Science (New York, NY) 153:1351–8

    Article  CAS  Google Scholar 

  • McGaugh JL (2000) Memory–a century of consolidation. Science (New York, NY) 287:248–51

    Article  CAS  Google Scholar 

  • McKenzie S, Eichenbaum H (2011) Consolidation and reconsolidation: two lives of memories? Neuron 71:224–33

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miki H, Suetsugu S, Takenawa T (1998) WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J 17:6932–41

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Monfils MH, Cowansage KK, Klann E, LeDoux JE (2009) Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science (New York, NY) 324:951–5

    Article  CAS  Google Scholar 

  • Nader K, Hardt O (2009) A single standard for memory: the case for reconsolidation. Nat Rev Neurosci 10:224–34

    Article  CAS  PubMed  Google Scholar 

  • Nader K, Schafe GE, Le Doux JE (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722–6

    Article  CAS  PubMed  Google Scholar 

  • Nobes CD, Hall A (1995) Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53–62

    Article  CAS  PubMed  Google Scholar 

  • Nomura H, Nonaka A, Imamura N, Hashikawa K, Matsuki N (2012) Memory coding in plastic neuronal subpopulations within the amygdala. NeuroImage 60:153–61

    Article  PubMed  Google Scholar 

  • Olshavsky ME, Song BJ, Powell DJ, Jones CE, Monfils MH, Lee HJ (2013) Updating appetitive memory during reconsolidation window: critical role of cue-directed behavior and amygdala central nucleus. Frontiers Behav Neurosci 7:186

    Google Scholar 

  • Pare D, Quirk GJ, Ledoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92:1–9

    Article  PubMed  Google Scholar 

  • Pitts MW, Todorovic C, Blank T, Takahashi LK (2009) The central nucleus of the amygdala and corticotropin-releasing factor: insights into contextual fear memory. J Neurosci: Official J Soc Neurosci 29:7379–88

    Article  CAS  Google Scholar 

  • Rajnicek AM, Foubister LE, McCaig CD (2006) Temporally and spatially coordinated roles for Rho, Rac, Cdc42 and their effectors in growth cone guidance by a physiological electric field. J Cell Sci 119:1723–35

    Article  CAS  PubMed  Google Scholar 

  • Rau V, DeCola JP, Fanselow MS (2005) Stress-induced enhancement of fear learning: an animal model of posttraumatic stress disorder. Neurosci Biobehav Rev 29:1207–23

    Article  PubMed  Google Scholar 

  • Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A (1992) The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70:401–10

    Article  CAS  PubMed  Google Scholar 

  • Roozendaal B, Schelling G, McGaugh JL (2008) Corticotropin-releasing factor in the basolateral amygdala enhances memory consolidation via an interaction with the beta-adrenoceptor-cAMP pathway: dependence on glucocorticoid receptor activation. J Neurosci: Off J Soc Neurosci 28:6642–51

    Article  CAS  Google Scholar 

  • Rudy JW, Huff NC, Matus-Amat P (2004) Understanding contextual fear conditioning: insights from a two-process model. Neurosci Biobehav Rev 28:675–85

    Article  CAS  PubMed  Google Scholar 

  • Sacchetti B, Lorenzini CA, Baldi E, Tassoni G, Bucherelli C (1999) Auditory thalamus, dorsal hippocampus, basolateral amygdala, and perirhinal cortex role in the consolidation of conditioned freezing to context and to acoustic conditioned stimulus in the rat. J Neurosci: Off J Soc Neurosci 19:9570–8

    CAS  Google Scholar 

  • Sah P, Faber ES, Lopez De Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–34

    CAS  PubMed  Google Scholar 

  • Sah P, Westbrook RF (2008) Behavioural neuroscience: the circuit of fear. Nature 454:589–90

    Article  CAS  PubMed  Google Scholar 

  • Sahai E, Marshall CJ (2002) RHO-GTPases and cancer. Nat Rev Cancer 2:133–42

    Article  PubMed  Google Scholar 

  • Sananbenesi F, Fischer A, Wang X, Schrick C, Neve R, Radulovic J, Tsai LH (2007) A hippocampal Cdk5 pathway regulates extinction of contextual fear. Nat Neurosci 10:1012–9

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schafe GE, LeDoux JE (2000) Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J Neurosci: Off J Soc Neurosci 20:RC96

    CAS  Google Scholar 

  • Si J, Yang J, Xue L, Yang C, Luo Y, Shi H, Lu L (2012) Activation of NF-kappaB in basolateral amygdala is required for memory reconsolidation in auditory fear conditioning. PloS One 7:e43973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stehberg J, Moraga-Amaro R, Salazar C, Becerra A, Echeverria C, Orellana JA, Bultynck G, Ponsaerts R, Leybaert L, Simon F, Saez JC, Retamal MA (2012) Release of gliotransmitters through astroglial connexin 43 hemichannels is necessary for fear memory consolidation in the basolateral amygdala. FASEB J: Off Publ Fed Am Soc Exp Biol 26:3649–57

    Article  CAS  Google Scholar 

  • Strekalova T, Zorner B, Zacher C, Sadovska G, Herdegen T, Gass P (2003) Memory retrieval after contextual fear conditioning induces c-Fos and JunB expression in CA1 hippocampus. Genes Brain Behav 2:3–10

    Article  CAS  PubMed  Google Scholar 

  • Tayler KK, Tanaka KZ, Reijmers LG, Wiltgen BJ (2013) Reactivation of neural ensembles during the retrieval of recent and remote memory. Curr Biol: CB 23:99–106

    Article  CAS  PubMed  Google Scholar 

  • Tejada-Simon MV, Villasana LE, Serrano F, Klann E (2006) NMDA receptor activation induces translocation and activation of Rac in mouse hippocampal area CA1. Biochem Biophys Res Commun 343:504–12

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thomas KL, Arroyo M, Everitt BJ (2003) Induction of the learning and plasticity-associated gene Zif268 following exposure to a discrete cocaine-associated stimulus. Eur J Neurosci 17:1964–72

    Article  PubMed  Google Scholar 

  • Vazdarjanova A, McGaugh JL (1999) Basolateral amygdala is involved in modulating consolidation of memory for classical fear conditioning. J Neurosci: Off J Soc Neurosci 19:6615–22

    CAS  Google Scholar 

  • von Hertzen LS, Giese KP (2005) Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci: Off J Soc Neurosci 25:1935–42

    Article  Google Scholar 

  • Wang XY, Zhao M, Ghitza UE, Li YQ, Lu L (2008) Stress impairs reconsolidation of drug memory via glucocorticoid receptors in the basolateral amygdala. J Neurosci: Off J Soc Neurosci 28:5602–10

    Article  CAS  Google Scholar 

  • Xue YX, Luo YX, Wu P, Shi HS, Xue LF, Chen C, Zhu WL, Ding ZB, Bao YP, Shi J, Epstein DH, Shaham Y, Lu L (2012) A memory retrieval-extinction procedure to prevent drug craving and relapse. Science (New York, NY) 336:241–5

    Article  CAS  Google Scholar 

  • Yang C, Liu JF, Chai BS, Fang Q, Chai N, Zhao LY, Xue YX, Luo YX, Jian M, Han Y, Shi HS, Lu L, Wu P, Wang JS (2013) Stress within a restricted time window selectively affects the persistence of long-term memory. PloS one 8:e59075

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yim AJ, Moraes CR, Ferreira TL, Oliveira MG (2006) Protein synthesis inhibition in the basolateral amygdala following retrieval does not impair expression of morphine-associated conditioned place preference. Behav Brain Res 171:162–9

    Article  CAS  PubMed  Google Scholar 

  • Zhu WL, Shi HS, Wang SJ, Wu P, Ding ZB, Lu L (2011) Hippocampal CA3 calcineurin activity participates in depressive-like behavior in rats. J Neurochem 117:1075–86

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Natural Science Foundation of China (no. 81201032, 31230033, and 8H1225009). The authors declare that they do not have any conflicts of interest (financial or otherwise) related to the data presented in this manuscript.

Author information

Authors and Affiliations

  1. National Institute on Drug Dependence, Peking University, 38, Xue Yuan Road, Beijing, 100191, China

    Ping Wu, Zeng-Bo Ding, Shi-Qiu Meng, Hao-Wei Shen, Shi-Chao Sun, Yi-Xiao Luo, Jian-Feng Liu, Lin Lu, Wei-Li Zhu & Jie Shi

  2. Institute of Mental Health, Peking University, Beijing, 100191, China

    Lin Lu

Authors
  1. Ping Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zeng-Bo Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shi-Qiu Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hao-Wei Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shi-Chao Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yi-Xiao Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jian-Feng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lin Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Wei-Li Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jie Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Wei-Li Zhu or Jie Shi.

Additional information

Ping Wu and Zeng-Bo Ding Equally contributed to this work

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, P., Ding, ZB., Meng, SQ. et al. Differential role of Rac in the basolateral amygdala and cornu ammonis 1 in the reconsolidation of auditory and contextual Pavlovian fear memory in rats. Psychopharmacology 231, 2909–2919 (2014). https://doi.org/10.1007/s00213-014-3462-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-014-3462-0

Keywords

Search

Navigation